The involvement of type IV pili and the phytochrome CphA in gliding motility, lateral motility and photophobotaxis of the cyanobacterium Phormidium lacuna

Lamparter, Tilman; J, Babian; Fröhlich, Katrin; Mielke, Marion; Weber, Nora; Wunsch, Nadja; Zais, Finn; Schulz, Kevin; Aschmann, Vera; N, Spohrer; Krauß, Norbert

doi:10.1371/journal.pone.0249509

Cited by 12 publications

(25 citation statements)

References 49 publications

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“…The most common architecture is the irregular fascicular thylakoid arrangement consisting of 4 to 15 parallel thylakoid membranes on cell cross-sections as documented in Crocosphaera, Gloeothece, or Annamia (Villanueva et al 2018, Mare s et al 2019b. Chroococcales seem to be the only group with the formation of long thick pili (Linhartov a et al 2021, Lamparter et al 2022, but this feature has to be resolved by detailed studies. Interestingly, many strains within Chroococcales thrive in an environment with higher mineral content, such as thermal mineral springs, brackish or saline waters, and many of them were found to be euryhaline.…”

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confidence: 99%

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis

Strunecký

Ivanova

Mareš

2023

Journal of Phycology

125

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Cyanobacterial taxonomy is facing a period of rapid changes thanks to the ease of 16S rRNA gene sequencing and established workflows for description of new taxa. Since the last comprehensive review of the cyanobacterial system in 2014 until 2021, at least 273 species in 140 genera were newly described. These taxa were mainly placed into previously defined orders and families although several new families were proposed. However, the classification of most taxa still relied on hierarchical relationships inherited from the classical morphological taxonomy. Similarly, the obviously polyphyletic orders such as Synechococcales and Oscillatoriales were left unchanged. In this study, the rising number of genomic sequences of cyanobacteria and well‐described reference strains allowed us to reconstruct a robust phylogenomic tree for taxonomic purposes. A less robust but better sampled 16S rRNA gene phylogeny was mapped to the phylogenomic backbone. Based on both these phylogenies, a polyphasic classification throughout the whole phylum of Cyanobacteria was created, with ten new orders and fifteen new families. The proposed system of cyanobacterial orders and families relied on a phylogenomic tree but still employed phenotypic apomorphies where possible to make it useful for professionals in the field. It was, however, confirmed that morphological convergence of phylogenetically distant taxa was a frequent phenomenon in cyanobacteria. Moreover, the limited phylogenetic informativeness of the 16S rRNA gene, resulting in ambiguous phylogenies above the genus level, emphasized the integration of genomic data as a prerequisite for the conclusive taxonomic placement of a vast number of cyanobacterial genera in the future.

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mentioning

confidence: 99%

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis

Strunecký

Ivanova

Mareš

2023

Journal of Phycology

125

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“…When we irradiated P. lacuna filaments on agar with light from the side to induce phototaxis, we found no directional movement towards the light (8). However, the microscope light from below or from a lightemitting diode from below induced photophobotaxis, that is, the movement of filaments towards the lighted zone and the filaments collected within the light spot.…”

Section: Introductionmentioning

confidence: 80%

“…In cyanobacteria, phototaxis has been described in single-celled species (5), whereas photophobotaxis has been described in filamentous Oscillatoriales (6). Both the cyanobacterial phototactic and photophobotactic movements are mediated by type IV pili (7,8), a transmembrane multiprotein complex that generates a moving force by expelling and retracting PilA protein threads.…”

Section: Introductionmentioning

confidence: 99%

“…Like other cyanobacteria, P. lacuna moves by twitching on agar and other surfaces. Like other Oscillatoriales, filaments also undergo a second type of motion that takes place in liquid medium, where filaments oscillate against each other in lateral direction (8). Through natural transformation, several genes encoding type IV pili components have been knocked out.…”

Section: Introductionmentioning

confidence: 99%

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Roles of phytochrome, PixJ, and photosynthesis in photophobotaxis of the filamentous cyanobacterium Phormidium lacuna

Lamparter,

Schwabenland,

Jelen

et al. 2023

Preprint

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Cyanobacterium Phormidium lacuna filaments move from dark to illuminated areas by twitching motility. Time-lapse recordings demonstrated that this photophobotaxis response was based on random movements with movement reversion at the light-dark border. The filaments in the illuminated area form a biofilm attached to the surface. The wild-type and two mutants, pixJ and cphA, were investigated for photophobotaxis at diverse wavelengths and intensities. CphA is a cyanobacterial phytochrome; PixJ is a biliprotein with a methyl-accepting chemotaxis domain and is regarded as a phototaxis photoreceptor. The cphA mutant exhibits reduced biofilm surface binding. The pixJ mutant was characterized by greater photophobotaxis sensitivity. Thus, PixJ is a negative photophobotaxis regulator and does not serve as a light direction sensor. 3-(3,4-dichlorophenyl)1,1-dimethylurea (DCMU) blocks electron transfer in PS II. At concentrations of 100 and 1000 µM DCMU, photophobotaxis was inhibited, whereas motility was not significantly affected. This specific effect indicates PS II’s central role in light-direction sensing. It is argued that the intracellular concentrations of regular photoreceptors, including CphA or PixJ, are too small for a filament to sense rapid light intensity changes in very weak light. Three arguments, specific inhibition by DCMU, broad spectral sensitivity, and sensitivity against weak light, support photosynthesis pigments use as photophobotaxis sensors.

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“…Slime secretion accompanies gliding motility in all species studied to date. Several studies have also shown that deletion of genes involved in slime biosynthesis or secretion abolishes gliding motility [23]. However, studying the relation between slime and motility is difficult, as most dyes staining slime also stain common substrates used in microscopy, such as agar and glass slides.…”

Section: Resultsmentioning

confidence: 99%

Cellular coordination underpins rapid reversals in gliding filamentous cyanobacteria and its loss results in plectonemes

Rosko,

Cremin,

Locatelli

et al. 2024

Preprint

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Gliding motility involves a characteristic back-and-forth movement of cells without flagella, and is seen in diverse bacteria. It is currently unknown how reversal dynamics in gliding motility are coordinated, especially in the case of multi-cellular, filamentous cyanobacteria. Here, we study gliding motility dynamics in a recently described species, capable of extensive gliding motility and collective, macro-structure formation. We find that gliding motility involves filaments rotating and translating through slime tubes, rather than on top of slime. On agar, filaments move back-and-forth on well-defined trajectories, where they display a characteristic speed profile, peaking in the middle of the trajectory. The time spent during each reversal displays a long-tailed distribution, with most reversals being almost instantaneous, while few involve a significant time of no movement. During reversals, individual cells remain mostly coordinated in their motion. Based on these experimental observations, we develop a biophysical model that incorporates cellular propulsive forces, the direction of which is decided by each cell based on mechano-sensing of their neighbors' motion. This model can capture experimental observations and predicts that loss of mechano-sensing can cause de-coordination of filament ends during reversals. In line with this prediction, we find instances of filaments becoming de-coordinated during reversals and that these instances are associated with plectoneme formation. The presented characterisation of filament movement dynamics and the corresponding physical model will inform future studies on individual and collective filament behaviours under different conditions.

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The involvement of type IV pili and the phytochrome CphA in gliding motility, lateral motility and photophobotaxis of the cyanobacterium Phormidium lacuna

Cited by 12 publications

References 49 publications

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis

An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis

Roles of phytochrome, PixJ, and photosynthesis in photophobotaxis of the filamentous cyanobacterium Phormidium lacuna

Cellular coordination underpins rapid reversals in gliding filamentous cyanobacteria and its loss results in plectonemes

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